Skip to main content
SpringerLink
Log in

Developmental origins of structural diversity in pollen walls of Compositae

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Compositae exhibit some of the most complex and diverse pollen grains in flowering plants. This paper reviews the evolutionary and developmental origins of this diversity in pollen structure using recent models based on the behaviour of colloids and formation of micelles in the differentiating microspore glycocalyx and primexine. The developmental model is consistent with observations of structures recovered by pollen wall dissolution. Pollen wall diversity in Compositae is inferred to result from small changes in the glycocalyx, for example ionic concentration, which trigger the self-assembly of highly diverse structures. Whilst the fine details of exine substructure are, therefore, not under direct genetic control, it is likely that genes establish differences in the glycocalyx which define the conditions for self-assembly. Because the processes described here for Compositae can account for some of the most complex exine structures known, it is likely that they also operate in pollen walls with much simpler organisation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Barnes SH, Blackmore S (1986) Some functional features during pollen development. In: Blackmore S, Ferguson IK (eds) Pollen and spores: form and function. Academic Press, London, pp 71–80

    Google Scholar 

  • Barnes SH, Blackmore S (1988) Pollen ontogeny in Catananche caerulea L. (Compositae: Lactuceae) II. Free microspore stage to the formation of the male germ unit. Ann Bot 62:615–623

    Google Scholar 

  • Blackmore S (1981) Palynology and intergeneric relationships in subtribe Hyoseridinae (Compositae: Lactuceae). Bot J Linn Soc 82:1–13

    Article  Google Scholar 

  • Blackmore S (1982) Palynology of subtribe Scorzonerinae (Compositae: Lactuceae) and its taxonomic significance. Grana 21:149–160

    Article  Google Scholar 

  • Blackmore S (1990) Sporoderm homologies and morphogenesis in land plants, with a discussion of Echinops sphaerocephala (Compositae). Pl Syst Evol (suppl 5):1–12

  • Blackmore S, Barnes SH (1985) Cosmos pollen ontogeny: a scanning electron microscope study. Protoplasma 126:91–99

    Article  Google Scholar 

  • Blackmore S, Barnes SH (1987) Pollen wall morphogenesis in Tragopogon porrifolius (Compositae: Lactuceae) and its taxonomic significance. Rev Palaeobot Palynol 52:233–246

    Article  Google Scholar 

  • Blackmore S, Barnes SH (1988) Pollen ontogeny in Catananche caerulea L. (Compositae: Lactuceae) I. Premeiotic phase to establishment of tetrads. Ann Bot 62:605–614

    Google Scholar 

  • Blackmore S, Claugher D (1987) Observations on the substructural organisation of the exine in Fagus sylvatica L. (Fagaceae) and Scorzonera hispanica L. (Compositae: Lactuceae). Rev Palaeobot Palynol 53:175–184

    Article  Google Scholar 

  • Blackmore S, Crane PR (1988) Systematic implications of pollen and spore ontogeny. In: Humphries CJ (ed) Ontogeny and systematics. Columbia University Press, New York, pp 83–115

    Google Scholar 

  • Blackmore S, Crane PR (1998) The evolution of apertures in the spores and pollen grains of embryophytes. In: Owens SJ, Rudall PJ (eds) Reproductive biology. Royal Botanic Gardens, Kew, pp 159–182

    Google Scholar 

  • Blackmore S, van Helvoort H, Punt W (1984) On the terminology, origins and functions of caveate pollen in the Compositae. Rev Palaeobot Palynol 43:293–301

    Article  Google Scholar 

  • Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 74:483–498

    Article  Google Scholar 

  • Blackmore S, Wortley AH, Skvarla JJ, Robinson H (2009) Evolution of pollen in the Compositae. In: Funk VA, Susanna A, Stuessy T, Bayer R (eds) Systematics, evolution and biogeography of the Compositae. IAPT, Vienna, Austria, pp 101–130

    Google Scholar 

  • Capito RM, Azevedo HS, Velichko YS, Mata A, Stupp SI (2008) Self-assembly of large and small molecules into hierarchically ordered sacs and membranes. Science 319:1812–1816

    Article  CAS  PubMed  Google Scholar 

  • Collinson ME, Hemsley AR, Taylor WA (1993) Sporopollenin exhibiting colloidal organization in spore walls. Grana Suppl 1:31–39

    Article  Google Scholar 

  • Dickinson HG (1976) Common factors in exine deposition. In: Ferguson IK, Muller J (eds) The evolutionary significance of the exine. Academic Press, London, pp 67–89

    Google Scholar 

  • Dickinson HG, Heslop-Harrison J (1968) Common mode of deposition for the sporopollenin of sexine and nexine. Nature 220:926–927

    Article  CAS  PubMed  Google Scholar 

  • Dickinson HG, Potter U (1976) The development of patterning in the alveolar sexine of Cosmos bipinnatus. New Phytol 76:543–550

    Article  Google Scholar 

  • Dickinson HG, Sheldon JM (1986) The generation of patterning at the plasma membrane of the young microspore of Lilium. In: Blackmore S, Ferguson JK (eds) Pollen and spores: form and function. Linn. Soc. Symp. Ser. 12, pp 1–17

  • Dover GA (1972) The organisation and polarity of pollen mother cells of Triticum aestivum. J Cell Sci 11:699–711

    CAS  PubMed  Google Scholar 

  • El-Ghazaly G (1982) Ontogeny of pollen wall of Leontodon autumnalis (Hypochoeridinae, Compositae). Grana 21:103–113

    Article  Google Scholar 

  • Erdtman G (1952) Pollen morphology and plant taxonomy: angiosperms. An introduction to palynology I. Almqvist and Wiksell, Stockholm

    Google Scholar 

  • Fitzgerald MA, Knox RB (1995) Initiation of primexine in freeze-substituted microspores of Brassica campestris. Sexual Pl Reprod 8:99–104

    Google Scholar 

  • Florence AT (1977) Biological meaning of micellization. In: Mittal KL (ed) Micellization, solubilization, and microemulsions. Plenum Press, New York, pp 42–62

    Google Scholar 

  • Funk VA, Bayer RJ, Keeley SC, Chan R, Watson L, Gemeinholzer B, Schilling E, Panero JL, Baldwin BG, Garcia-Jacas N, Susanna A, Jansen RK (2005) Everywhere but Antarctica: using a supertree to understand the diversity and distribution of the Compositae. Biol Skr 55:343–374

    Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2002) Exine development in Stangeria eriopus (Stangeriaceae): ultrastructure and substructure, sporopollenin accumulation, the equivocal character of the aperture, and stereology of microspore organelles. Rev Palaeobot Palynol 122:185–218

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2003) Comparative study of the pollen wall development in Illicium floridanum (Illiciaceae) and Schisandra chinensis (Schisandraceae). Taiwania 48:147–167

    Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2004) Exine development in Encephalartos altensteinii (Cycadaceae): ultrastructure, substructure and the models of sporopollenin accumulation. Rev Palaeobot Palynol 132:175–193

    Article  Google Scholar 

  • Gabarayeva NI, Hemsley AR (2006) The role of self-assembly in the development of pollen wall structure. Rev Palaeobot Palynol 138:121–139

    Article  Google Scholar 

  • Gabarayeva NI, Blackmore S, Rowley JR (2003) Observations on the experimental destruction of the pollen wall of some selected gymnosperms and angiosperms. Rev Palaeobot Palynol 124:203–226

    Article  Google Scholar 

  • Hemsley AR (1998) Nonlinear variation in simulated complex pattern development. J Theor Biol 192:73–79

    Article  PubMed  Google Scholar 

  • Hemsley AR, Gabarayeva N (2007) Exine development: the importance of looking through a colloid chemistry “window”. Pl Syst Evol 263:25–49

    Article  Google Scholar 

  • Hemsley AR, Collinson ME, Brain APR (1992) Colloidal crystal-like structure of sporopollenin in the megaspore walls of recent Selaginella and similar fossil spores. Bot J Linn Soc 108:307–320

    Article  Google Scholar 

  • Hemsley AR, Griffiths PC, Matthias R, Moore SEM (2003) A model for the role of surfactants in the assembly of exine structure. Grana 42:38–42

    Article  Google Scholar 

  • Heslop-Harrison J (1963) An ultrastructural study of pollen wall ontogeny in Silene pendula. Grana Palynol 4:7–24

    Article  Google Scholar 

  • Heslop-Harrison J (1968) The pollen grain wall. Science 161:230–237

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison J (1969) The origin of surface features of the pollen wall of Tagetes patula as observed by scanning electron microscopy. Cytobios 2:177–186

    Google Scholar 

  • Heslop-Harrison J (1971) Wall pattern formation in angiosperm microsporogenesis. Symp Soc Exp Biol 25:277–300

    CAS  PubMed  Google Scholar 

  • Heslop-Harrison J (1972) Pattern in plant cell walls: morphogenesis in miniature. Proc Roy Inst Gr Brit 45:335–351

    Google Scholar 

  • Heslop-Harrison J (1979) Pollen walls as adaptive systems. Ann Missouri Bot Gard 66:813–829

    Article  Google Scholar 

  • Horner HT, Pearson CB (1978) Pollen wall and aperture development in Helianthus annuus (Compositae: Heliantheae). Amer J Bot 65:293–309

    Article  Google Scholar 

  • Jackson RC, Skvarla JJ, Chissoe WF (2000) A unique pollen wall mutation in the family Compositae: ultrastructure and genetics. Amer J Bot 87:1571–1577

    Article  Google Scholar 

  • Longly B, Waterkeyn L (1979) Etude de la cytocinese. III. Les cloisonnements simultanés et successifs des microsporocytes. Cellule 73:65–80

    Google Scholar 

  • Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434

    Article  CAS  PubMed  Google Scholar 

  • McCormick S (2004) Control of male gametophyte development. Plant Cell 16:S142–S153

    Article  CAS  PubMed  Google Scholar 

  • Nazarova EA (1997) Karyosystematic investigation of the genus Scorzonera L. s.l. (Lactuceae, Asteraceae). Caryologia 50:239–261

    Google Scholar 

  • Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Haynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185:7–21

    Article  Google Scholar 

  • Paxson-Sowders DM, Owen HA, Makaroff CA (1997) A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation. Protoplasma 198:53–65

    Article  Google Scholar 

  • Paxson-Sowders DM, Dodrill CJ, Owen HA, Makaroff CA (2001) DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol 127:1739–1749

    Article  CAS  PubMed  Google Scholar 

  • Pettitt JM (1979) Ultrastructure and cytochemistry of spore wall morphogenesis. In: Dyer AF (ed) The experimental biology of ferns. Academic Press, London, pp 211–252

    Google Scholar 

  • Pettitt JM, Jermy AC (1974) The surface coats on spores. Biol J Linn Soc 6:245–257

    Article  Google Scholar 

  • Rowley JR (1971) Implications on the nature of sporopollenin based upon pollen development. In: Brooks J, Grant PR, Muir M, van Gijzel P, Shaw G (eds) Sporopollenin. Academic Press, London, pp 174–219

    Google Scholar 

  • Rowley JR (1973) Formation of pollen exine bacules and microchannels on a glycocalyx. Grana 13:129–138

    Article  Google Scholar 

  • Rowley JR (1980) The origin, ontogeny and evolution of the exine. Proceedings of the IVth International Palynological Conference, Lucknow, 1976–1977. 1:126–136

  • Rowley JR (1990) The fundamental structure of the exine. Pl Syst Evol (Suppl. 5):13–29

  • Rowley JR, Claugher D (1991) Receptor-independent sporopollenin. Bot Acta 104:316–323

    Google Scholar 

  • Rowley JR, Dahl AO (1977) Pollen development in Artemisa vulgaris with special reference to glycoclayx material (1). Pollen Spores 14:169–284

    Google Scholar 

  • Rowley JR, Prijianto B (1977) Selective destruction of the exine of pollen grains. Geophytol 7:1–23

    Google Scholar 

  • Rowley JR, Skvarla JJ (1975) The glycocalyx and initiation of exine spinules on microspores of Canna. Amer J Bot 62:479–485

    Article  Google Scholar 

  • Rowley JR, Skvarla JJ (1993) Exine receptors. Grana 2:21–25

    Article  Google Scholar 

  • Rowley JR, Skvarla JJ (2007) Pollen development in Epilobium (Onagraceae): from microspore mitosis to formation of the intine. Grana 46:130–139

    Article  Google Scholar 

  • Rowley JR, Southworth D (1967) Deposition of sporopollenin on lamellae of unit membrane dimensions. Nature 213:703–704

    Article  Google Scholar 

  • Rowley JR, Dahl AO, Rowley JS (1981) Substructure in exines of Artemisia vulgaris (Asteraceae). Rev Palaeobot Palynol 35:1–38

    Article  Google Scholar 

  • Rowley JR, Claugher D, Skvarla JJ (1999a) Structure of the exine in Artemisia vulgaris (Asteraeae): a review. Taiwania 44:1–21

    Google Scholar 

  • Rowley JR, Skvarla JJ, Gabarayeva NI (1999b) Exine development in Borago (Boraginaceae): 2. Free microspore stages. Taiwania 44:212–229

    Google Scholar 

  • Rowley JR, Skvarla JJ, Walles B (1999c) Microsporogenesis in Pinus sylvestris.—VII. Exine expansion and tapetal development. Taiwania 44:325–344

    Google Scholar 

  • Scott RJ (1994) Pollen exine—the sporopollenin enigma and the physics of pattern. In: Scott RJ, Stead MA (eds) Society for experimental biology seminar series 55: molecular and cellular aspects of plant reproduction. Cambridge University Press, Cambridge, pp 49–81

    Google Scholar 

  • Sheldon JM, Dickinson HG (1983) Determination of patterning in the pollen wall in Lilium henryi. J Cell Sci 63:191–208

    CAS  PubMed  Google Scholar 

  • Skvarla JJ, Larson DA (1965) An electron microscopic study of pollen morphology in the Compositae with special reference to the Ambrosiinae. Grana 6:210–269

    Article  Google Scholar 

  • Skvarla JJ, Turner BL (1966) Systematic implications from electron microscopic studies of Compositae pollen—a review. Ann Missouri Bot Gard 53:220–256

    Article  Google Scholar 

  • Skvarla JJ, Turner BL, Patel VC, Tomb AS (1977) Pollen morphology in the Compositae and in morphologically related families. In: Heywood VH, Harborne JB, Turner BL (eds) The biology and chemistry of the Compositae. Academic Press, London, pp 141–248

    Google Scholar 

  • Skvarla JJ, Rowley JR, Chissoe WF, Strout G (2001) Incomplete exine development in aborted pollen of Eupatorium serotinum Michx. (Compositae: Eupatorieae). Taiwania 46:103–113

    Google Scholar 

  • Southworth D (1974) Solubility of pollen exines. Amer J Bot 61:36–44

    Article  Google Scholar 

  • Southworth D (1983) Exine development in Gerbera jamesonii (Asteraceae: Mutisieae). Amer J Bot 70:1038–1047

    Article  Google Scholar 

  • Southworth D (1986) Substructural organization of pollen exines. In: Blackmore S, Ferguson IK (eds) Pollen and spores: form and function. Academic Press, London, pp 61–69

    Google Scholar 

  • Southworth D, Jernstedt JA (1995) Pollen exine development precedes microtubule rearrangement in Vigna unguiculata (Fabaceae): a model for pollen wall patterning. Protoplasma 187:79–87

    Article  Google Scholar 

  • Stix E (1960) Pollenmorphologische Untersuchungen an Compositen. Grana 2:41–104

    Article  Google Scholar 

  • Takahashi M (1989) Development of the echinate pollen wall in Farfugium japonicum (Compositae: Senecioneae). Bot Mag (Tokyo) 102:219–234

    Article  Google Scholar 

  • Thomson DA (1917) On growth and form. Cambridge University Press, Cambridge

    Google Scholar 

  • Tomb AS, Larson DA, Skvarla JJ (1974) Pollen morphology and detailed structure of family Compositae, tribe Cichorieae. I. Subtribe Stephanomeriinae. Amer J Bot 61:486–498

    Article  Google Scholar 

  • Turner BL (1977) Summary of the biology of the Compositae. In: Heywood VH, Harborne JB, Turner BL (eds) The biology and chemistry of the Compositae. Academic Press, London, pp 1105–1118

    Google Scholar 

  • Varotto S, Parrini P, Mariani P (1996) Pollen ontogeny in Cichorium intybus L. Grana 35:154–161

    Article  Google Scholar 

  • Wagenitz G (1955) Pollenmorphologie und Systematik in der Gattung Centaurea L. s.l. Flora 142:213–279

    Google Scholar 

  • Wagenitz G (1976) Systematics and phylogeny of the Compositae. Pl Syst Evol 125:29–46

    Article  Google Scholar 

  • Wodehouse RP (1930) Pollen grains in the identification and classification of plants. V. Haplopappus and other Astereae: the origin of their furrow configurations. Amer J Bot 16:297–313

    Article  Google Scholar 

  • Wodehouse RP (1931) The origin of the six-furrowed configuration of Dahlia pollen grains. Bull Torrey Bot Club 57:371–380

    Article  Google Scholar 

  • Wodehouse RP (1935) Pollen grains: their structure, identification and significance in science and medicine. McGraw–Hill Book Company, Inc., New York

    Google Scholar 

  • Wortley AH, Blackmore S, Skvarla JJ (2009) Bibliography of pollen literature in the Compositae. In: Funk VA, Susanna A, Stuessy T, Bayer R (eds) Systematics, Evolution and biogeography of the Compositae. IAPT, Vienna, Austria, pp 807–867

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to Donald Claugher and Susan H. Barnes for helping to shape our ideas about pollen development and exine ontogeny. This paper was first conceived as part of a Festschrift in honour of Gerhard Wagenitz; we thank the organisers and Professor Wagenitz himself for their inspiration.

Author information

Authors and Affiliations

  1. Royal Botanic Garden Edinburgh, 20a Inverleith Row, Edinburgh, EH3 5LR, Scotland, UK

    Stephen Blackmore & Alexandra H. Wortley

  2. Department of Botany and Microbiology, University of Oklahoma, Norman, OK, 73019-0245, USA

    John J. Skvarla

  3. Komarov Botanical Institute, Popov Street 2, St Petersburg, 197376, Russian Federation

    Nina I. Gabarayeva

  4. Botany Department, University of Stockholm, 106 91, Stockholm, Sweden

    John R. Rowley

Authors
  1. Stephen Blackmore
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexandra H. Wortley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John J. Skvarla
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nina I. Gabarayeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John R. Rowley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen Blackmore.

Additional information

This paper is dedicated to the memory of Donald Claugher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blackmore, S., Wortley, A.H., Skvarla, J.J. et al. Developmental origins of structural diversity in pollen walls of Compositae. Plant Syst Evol 284, 17–32 (2010). https://doi.org/10.1007/s00606-009-0232-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-009-0232-2

Keywords

Search

Navigation